CHK1 inhibition in small-cell lung cancer produces single-agent activity in biomarker-defined disease subsets and combination activity with cisplatin or olaparib

Cancer Research

Volumn 77, Issue 14, 2017, Pages 3870-3884

  Sen, Triparna ^a   Tong, Pan ^a   Stewart, C Allison ^a   Cristea, Sandra ^b   Valliani, Aly ^a   Shames, David S ^c   Redwood, Abena B ^a   Fan, You Hong ^a   Li, Lerong ^a   Glisson, Bonnie S ^a   Minna, John D ^d   Sage, Julien ^b   Gibbons, Don L ^a   Piwnica Worms, Helen ^a   Heymach, John V ^a   Wang, Jing ^a   Byers, Lauren Averett ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b STANFORD UNIVERSITY   (United States)

^c GENENTECH INC   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; CISPLATIN; MYC PROTEIN; OLAPARIB; PREXASERTIB; RNA; ANTINEOPLASTIC AGENT; CHEK1 PROTEIN, MOUSE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PHTHALAZINE DERIVATIVE; PIPERAZINE DERIVATIVE; PYRAZINE DERIVATIVE; PYRAZOLE DERIVATIVE; TUMOR MARKER;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MEGADOSE; DRUG TARGETING; ENZYME INHIBITION; FEMALE; GENE AMPLIFICATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LOW DRUG DOSE; MALE; MOUSE; NONHUMAN; ONCOGENE MYC; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RNA INTERFERENCE; SMALL CELL LUNG CANCER; YOUNG ADULT; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG POTENTIATION; ENZYMOLOGY; GENE SILENCING; GENETICS; LUNG NEOPLASMS; METABOLISM; NUDE MOUSE; PATHOLOGY; SMALL CELL LUNG CARCINOMA; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BIOMARKERS, TUMOR; CELL LINE, TUMOR; CHECKPOINT KINASE 1; CISPLATIN; DRUG SYNERGISM; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; LUNG NEOPLASMS; MICE; MICE, NUDE; PHTHALAZINES; PIPERAZINES; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; PYRAZINES; PYRAZOLES; SMALL CELL LUNG CARCINOMA;

EID: 85023745986     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-3409     Document Type: Article

References (44)

1. Govindan R, Page N, Morgensztern D, Read W, Tierney R, Vlahiotis A, et al. Changing epidemiology of small-cell lung cancer in the United States over the last 30 years: analysis of the surveillance, epidemiologic, and end results database. J Clin Oncol 2006;24:4539–44
2. William WN Jr, Glisson BS. Novel strategies for the treatment of small-cell lung carcinoma. Nat Rev Clin Oncol 2011;8:611–9
3. Byers LA, Rudin CM. Small cell lung cancer: where do we go from here? Cancer 2015;121:664–72
4. Kim YH, Girard L, Giacomini CP, Wang P, Hernandez-Boussard T, Tibshirani R, et al. Combined microarray analysis of small cell lung cancer reveals altered apoptotic balance and distinct expression signatures of MYC family gene amplification. Oncogene 2006;25:130–8
5. George J, Lim JS, Jang SJ, Cun Y, Ozretic L, Kong G, et al. Comprehensive genomic profiles of small cell lung cancer. Nature 2015;524:47–53
6. Peifer M, Fernandez-Cuesta L, Sos ML, George J, Seidel D, Kasper LH, et al. Integrative genome analyses identify key somatic driver mutations of small-cell lung cancer. Nat Genet 2012;44:1104–10
7. Rudin CM, Durinck S, Stawiski EW, Poirier JT, Modrusan Z, Shames DS, et al. Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer. Nat Genet 2012; 44:1111–6
8. Sato M, Shames DS, Gazdar AF, Minna JD. A translational view of the molecular pathogenesis of lung cancer. J Thorac Oncol 2007;2:327–43
9. Jahchan NS, Lim JS, Bola B, Morris K, Seitz G, Tran KQ, et al. Identification and targeting of long-term tumor-propagating cells in small cell lung cancer. Cell Rep 2016;16:644–56
10. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004;304:1497–500
11. Pao W, Chmielecki J. Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer. Nat Rev Cancer 2010;10:760–74
12. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 2007;448:561–6
13. Byers LA, Wang J, Nilsson MB, Fujimoto J, Saintigny P, Yordy J, et al. Proteomic profiling identifies dysregulated pathways in small cell lung cancer and novel therapeutic targets including PARP1. Cancer Discov 2012;2:798–811
14. Bunn PA Jr., Minna JD, Augustyn A, Gazdar AF, Ouadah Y, Krasnow MA, et al. Small cell lung cancer: can recent advances in biology and molecular biology be translated into improved outcomes? J Thorac Oncol 2016;11: 453–74
15. Booth L, Cruickshanks N, Ridder T, Dai Y, Grant S, Dent P. PARP and CHK inhibitors interact to cause DNA damage and cell death in mammary carcinoma cells. Cancer Biol Ther 2013;14:458–65
16. Karnak D, Engelke CG, Parsels LA, Kausar T, Wei D, Robertson JR, et al. Combined inhibition of Wee1 and PARP1/2 for radiosensitization in pancreatic cancer. Clin Cancer Res 2014;20:5085–96
17. Gadhikar MA, Sciuto MR, Alves MV, Pickering CR, Osman AA, Neskey DM, et al. Chk1/2 inhibition overcomes the cisplatin resistance of head and neck cancer cells secondary to the loss of functional p53. Mol Cancer Ther 2013;12:1860–73
18. Ma CX, Cai S, Li S, Ryan CE, Guo Z, Schaiff WT, et al. Targeting Chk1 in p53-deficient triple-negative breast cancer is therapeutically beneficial in human-in-mouse tumor models. J Clin Invest 2012;122:1541–52
19. Ma CX, Janetka JW, Piwnica-Worms H. Death by releasing the breaks: CHK1 inhibitors as cancer therapeutics. Trends Mol Med 2011;17:88–96
20. Zhang Y, Hunter T. Roles of Chk1 in cell biology and cancer therapy. Int J Cancer 2014;134:1013–23
21. Christensen CL, Kwiatkowski N, Abraham BJ, Carretero J, Al-Shahrour F, Zhang T, et al. Targeting transcriptional addictions in small cell lung cancer with a covalent CDK7 inhibitor. Cancer Cell 2014;26:909–22
22. Hong D, Infante J, Janku F, Jones S, Nguyen LM, Burris H, et al. Phase I study of LY2606368, a checkpoint kinase 1 inhibitor, in patients with advanced cancer. J Clin Oncol 2016
23. Jahchan NS, Dudley JT, Mazur PK, Flores N, Yang D, Palmerton A, et al. A drug repositioning approach identifies tricyclic antidepressants as inhibitors of small cell lung cancer and other neuroendocrine tumors. Cancer Discov 2013;3:1364–77
24. Schaffer BE, Park KS, Yiu G, Conklin JF, Lin C, Burkhart DL, et al. Loss of p130 accelerates tumor development in a mouse model for human small-cell lung carcinoma. Cancer Res 2010;70:3877–83
25. Masters JR, Thomson JA, Daly-Burns B, Reid YA, Dirks WG, Packer P, et al. Short tandem repeat profiling provides an international reference standard for human cell lines. Proc Nat Acad Sci U S A 2001;98:8012–7
26. Gazdar AF, Savage TK, Johnson JE, Berns A, Sage J, Linnoila RI, et al. The comparative pathology of genetically engineered mouse models for neuroendocrine carcinomas of the lung. J Thorac Oncol 2015;10: 553–64
27. Tong P, Coombes KR, Johnson FM, Byers LA, Diao L, Liu DD, et al. drexplorer: A tool to explore dose-response relationships and drug-drug interactions. Bioinformatics 2015;31:1692–4
28. Prichard MN, Shipman C .A three-dimensional model to analyze drug-drug interactions. Antiviral Res 1990;14:181–205
29. R Development Core Team. R Development Core Team (2011), R: A Language and Environment for Statistical Computing. Vienna, Austria: the R Foundation for Statistical Computing: R Foundation for Statistical Computing; 2011.
30. King C, Diaz HB, McNeely S, Barnard D, Dempsey J, Blosser W, et al. LY2606368 causes replication catastrophe and antitumor effects through CHK1-dependent mechanisms. Mol Cancer Ther 2015;14:2004–13
31. Twentyman PR, Wright KA, Mistry P, Kelland LR, Murrer BA. Sensitivity to novel platinum compounds of panels of human lung cancer cell lines with acquired and inherent resistance to cisplatin. Cancer Res 1992;52:5674–80
32. Cardnell RJ, Feng Y, Mukherjee S, Diao L, Tong P, Stewart CA, et al. Activation of the PI3K/mTOR pathway following PARP inhibition in small cell lung cancer. PLoS ONE 2016;11:e0152584
33. Cardnell RJ, Feng Y, Diao L, Fan YH, Masrorpour F, Wang J, et al. Proteomic markers of DNA repair and PI3K pathway activation predict response to the PARP inhibitor BMN 673 in small cell lung cancer. Clin Cancer Res 2013;19:6322–8
34. Polley E, Kunkel M, Evans D, Silvers T, Delosh R, Laudeman J, et al. Small cell lung cancer screen of oncology drugs, investigational agents, and gene and microRNA expression. J Nat Cancer Inst 2016;108:djw122. doi: 10.1093/jnci/djw122.
35. Tong P, Chen Y, Su X, Coombes KR. SIBER: systematic identification of bimodally expressed genes using RNAseq data. Bioinformatics 2013;29: 605–13
36. Wang J, Wen S, Symmans WF, Pusztai L, Coombes KR. The bimodality index: a criterion for discovering and ranking bimodal signatures from cancer gene expression profiling data. Cancer Inform 2009;7:199–216
37. Hermeking H. The 14-3-3 cancer connection. Nat Rev Cancer 2003;3: 931–43
38. Stoimenov I, Helleday T. PCNA on the crossroad of cancer. Biochem Soc Trans 2009;37:605–13
39. Toledo LI, Murga M, Fernandez-Capetillo O. Targeting ATR and Chk1 kinases for cancer treatment: a new model for new (and old) drugs. Mol Oncol 2011;5:368–73
40. Thompson R, Meuth M, Woll P, Zhu Y, Danson S. Treatment with the Chk1 inhibitor Go6976 enhances cisplatin cytotoxicity in SCLC cells. Int J Oncol 2012;40:194–202
41. Mitchell C, Park M, Eulitt P, Yang C, Yacoub A, Dent P. Poly(ADP-ribose) polymerase 1 modulates the lethality of CHK1 inhibitors in carcinoma cells. Mol Pharmacol 2010;78:909–17
42. Murga M, Campaner S, Lopez-Contreras AJ, Toledo LI, Soria R, Montana MF, et al. Exploiting oncogene-induced replicative stress for the selective killing of Myc-driven tumors. Nat Struct Mol Biol 2011;18:1331–5
43. Hoglund A, Nilsson LM, Muralidharan SV, Hasvold LA, Merta P, Rudelius M, et al. Therapeutic implications for the induced levels of Chk1 in Myc-expressing cancer cells. Clin Cancer Res 2011;17:7067–79
44. Wang WJ, Wu SP, Liu JB, Shi YS, Huang X, Zhang QB, et al. MYC regulation of CHK1 and CHK2 promotes radioresistance in a stem cell-like population of nasopharyngeal carcinoma cells. Cancer Res 2013; 73:1219–31